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Advances in the aquatic sciences
RESEARCH ARTICLE

Direct and indirect effects of near-future pCO2 levels on zooplankton dynamics

Cédric L. Meunier A C , María Algueró-Muñiz A , Henriette G. Horn A , Julia A. F. Lange A and Maarten Boersma A B
+ Author Affiliations
- Author Affiliations

A Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und Meeresforschung, Biologische Anstalt Helgoland, Postfach 180, D-27483 Helgoland, Germany.

B University of Bremen, D-28359 Bremen, Germany.

C Corresponding author. Email: cedric.meunier@awi.de

Marine and Freshwater Research 68(2) 373-380 https://doi.org/10.1071/MF15296
Submitted: 3 August 2015  Accepted: 22 December 2015   Published: 21 March 2016

Abstract

Ocean acidification has direct physiological effects on organisms, for example by dissolving the calcium carbonate structures of calcifying species. However, non-calcifiers may also be affected by changes in seawater chemistry. To disentangle the direct and indirect effects of ocean acidification on zooplankton growth, we undertook a study with two model organisms. Specifically, we investigated the individual effects of short-term exposure to high and low seawater pCO2, and different phytoplankton qualities as a result of different CO2 incubations on the growth of a heterotrophic dinoflagellate (Oxyrrhis marina) and a copepod species (Acartia tonsa). It was observed previously that higher CO2 concentrations can decrease phytoplankton food quality in terms of carbon : nutrient ratios. We therefore expected both seawater pCO2 (pH) and phytoplankton quality to result in decreased zooplankton growth. Although we expected lowest growth rates for all zooplankton under high seawater pCO2 and low algal quality, we found that direct pH effects on consumers seem to be of lesser importance than the associated decrease in algal quality. The decrease in the quality of primary producers under high pCO2 conditions negatively affected zooplankton growth, which may lead to lower availability of food for the next trophic level and thus potentially affect the recruitment of higher trophic levels.

Additional keywords: copepod, dinoflagellate, ecological stoichiometry, food web, microzooplankton, ocean acidification.


References

Aberle, N., Schulz, K. G., Stuhr, A., Malzahn, A. M., Ludwig, A., and Riebesell, U. (2013). High tolerance of microzooplankton to ocean acidification in an Arctic coastal plankton community. Biogeosciences 10, 1471–1481.
High tolerance of microzooplankton to ocean acidification in an Arctic coastal plankton community.Crossref | GoogleScholarGoogle Scholar |

Bradshaw, A. L., Brewer, P. G., Shafer, D. K., and Williams, R. T. (1981). Measurements of total carbon dioxide and alkalinity by potentiometric titration in the GEOSECS program. Earth and Planetary Science Letters 55, 99–115.
Measurements of total carbon dioxide and alkalinity by potentiometric titration in the GEOSECS program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtV2hsro%3D&md5=aefe1f6a10e75f29b23404453ac5db81CAS |

Burkhardt, S., Zondervan, I., and Riebesell, U. (1999). Effect of CO2 concentration on C : N : P ratio in marine phytoplankton: a species comparison. Limnology and Oceanography 44, 683–690.
Effect of CO2 concentration on C : N : P ratio in marine phytoplankton: a species comparison.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1yjs7g%3D&md5=9f2f4198ea85dcbb2849aa7df2b539deCAS |

Canadell, J. G., Le Quéré, C., Raupach, M. R., Field, C. B., Buitenhuis, E. T., Ciais, P., Conway, T. J., Gillett, N. P., Houghton, R. A., and Marland, G. (2007). Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences of the United States of America 104, 18866–18870.
Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2ks7%2FO&md5=68d095a129341dd9f02e89df7aab8b93CAS | 17962418PubMed |

Caron, D. A., and Hutchins, D. A. (2013). The effects of changing climate on microzooplankton grazing and community structure: drivers, predictions and knowledge gaps. Journal of Plankton Research 35, 235–252.
The effects of changing climate on microzooplankton grazing and community structure: drivers, predictions and knowledge gaps.Crossref | GoogleScholarGoogle Scholar |

Cripps, G., Lindeque, P., and Flynn, K. (2014a). Parental exposure to elevated pCO2 influences the reproductive success of copepods. Journal of Plankton Research 36, 1165–1174.
Parental exposure to elevated pCO2 influences the reproductive success of copepods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslGgtLvP&md5=4fc6dc32aba332934dc429f465d626bcCAS | 25221371PubMed |

Cripps, G., Lindeque, P., and Flynn, K. J. (2014b). Have we been underestimating the effects of ocean acidification in zooplankton? Global Change Biology 20, 3377–3385.
Have we been underestimating the effects of ocean acidification in zooplankton?Crossref | GoogleScholarGoogle Scholar | 24782283PubMed |

Davidson, K., Sayegh, F., and Montagnes, D. J. S. (2011). Oxyrrhis marina-based models as a tool to interpret protozoan population dynamics. Journal of Plankton Research 33, 651–663.
Oxyrrhis marina-based models as a tool to interpret protozoan population dynamics.Crossref | GoogleScholarGoogle Scholar |

Dickson, A. G., and Millero, F. J. (1987). A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research – A. Oceanographic Research Papers 34, 1733–1743.
A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXotFGjsg%3D%3D&md5=a7061575b13208e16fea0840d16a32f0CAS |

Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. (2009). Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169–192.
Ocean acidification: the other CO2 problem.Crossref | GoogleScholarGoogle Scholar | 21141034PubMed |

Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C. (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65, 414–432.
Impacts of ocean acidification on marine fauna and ecosystem processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFegtL4%3D&md5=a82ec107f768c7cc820034735b8729edCAS |

Flynn, K. J., Blackford, J. C., Baird, M. E., Raven, J. A., Clark, D. R., Beardall, J., Brownlee, C., Fabian, H., and Wheeler, G. L. (2012). Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change 2, 510–513.
Changes in pH at the exterior surface of plankton with ocean acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVGiu7w%3D&md5=956151254fcb118da352d4eb70b3a884CAS |

Flynn, K. J., Clark, D. R., Mitra, A., Fabian, H., Hansen, P. J., Glibert, P. M., Wheeler, G. L., Stoecker, D. K., Blackford, J. C., and Brownlee, C. (2015). Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession. Proceedings of the Royal Society of London – B. Biological Sciences 282, 20142604.
Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession.Crossref | GoogleScholarGoogle Scholar |

Grasshoff, K., Ehrhardt, M., and Kremling, K. (1999). ‘Methods of Seawater Analysis.’ (Wiley-VCH. Weinheim, Germany)

Grizzetti, B., Bouraoui, F., and Aloe, A. (2012). Changes of nitrogen and phosphorus loads to European seas. Global Change Biology 18, 769–782.
Changes of nitrogen and phosphorus loads to European seas.Crossref | GoogleScholarGoogle Scholar |

Guillard, R. R. L., and Ryther, J. H. (1962). Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Canadian Journal of Microbiology 8, 229–239.
Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XktlWqu70%3D&md5=af43e682fb8b2db5618d5a613f49e2eeCAS |

Hinga, K. R. (2002). Effects of pH on coastal marine phytoplankton. Marine Ecology Progress Series 238, 281–300.
Effects of pH on coastal marine phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Isari, S., Zervoudaki, S., Peters, J., Papantoniou, G., Pelejero, C., and Saiz, E. (2016). Lack of evidence for elevated CO2-induced bottom-up effects on marine copepods: a dinoflagellate–calanoid prey–predator pair. ICES Journal of Marine Science 73, 650–658.
Lack of evidence for elevated CO2-induced bottom-up effects on marine copepods: a dinoflagellate–calanoid prey–predator pair.Crossref | GoogleScholarGoogle Scholar |

Klein Breteler, W. C. M., Schogt, N., Baas, M., Schouten, S., and Kraay, G. W. (1999). Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Marine Biology 135, 191–198.
Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids.Crossref | GoogleScholarGoogle Scholar |

Kurihara, H., Shimode, S., and Shirayama, Y. (2004). Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea). Marine Pollution Bulletin 49, 721–727.
Effects of raised CO2 concentration on the egg production rate and early development of two marine copepods (Acartia steueri and Acartia erythraea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVKjsbk%3D&md5=e81a64bdecd7b2c309f3e71c1ab08b44CAS | 15530515PubMed |

Lewis, E., and Wallace, D. (1998). ‘Program Developed for CO2 System Calculations.’ (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy: Oak Ridge, TN.)

Lewis, C. N., Brown, K. A., Edwards, L. A., Cooper, G., and Findlay, H. S. (2013). Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice. Proceedings of the National Academy of Sciences of the United States of America 110, E4960–E4967.
Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnsV2gsw%3D%3D&md5=7db418b42fd8dd9ccc3a9b919bce2578CAS | 24297880PubMed |

Low-Décarie, E., Fussmann, G. F., and Bell, G. (2014). Aquatic primary production in a high-CO2 world. Trends in Ecology & Evolution 29, 223–232.
Aquatic primary production in a high-CO2 world.Crossref | GoogleScholarGoogle Scholar |

Malzahn, A. M., Aberle, N., Clemmesen, C., and Boersma, M. (2007). Nutrient limitation of primary producers affects planktivorous fish condition. Limnology and Oceanography 52, 2062–2071.
Nutrient limitation of primary producers affects planktivorous fish condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ahsLvK&md5=443947adbe0c0fe9df40a64da33611bcCAS |

Mauchline, J. (1988). The biology of calanoid copepods. In ‘Advances in Marine Biology’. pp. 1–143. (Academic Press: New York)

Mayor, D., Matthews, C., Cook, K., Zuur, A., and Hay, S. (2007). CO2-induced acidification affects hatching success in Calanus finmarchicus. Marine Ecology Progress Series 350, 91–97.
CO2-induced acidification affects hatching success in Calanus finmarchicus.Crossref | GoogleScholarGoogle Scholar |

Mayor, D. J., Everett, N. R., and Cook, K. B. (2012). End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod. Journal of Plankton Research 34, 258–262.
End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XisVGqtrk%3D&md5=8038f65c84a2640064d6c18c98a9bbfaCAS |

McConville, K., Halsband, C., Fileman, E. S., Somerfield, P. J., Findlay, H. S., and Spicer, J. I. (2013). Effects of elevated CO2 on the reproduction of two calanoid copepods. Marine Pollution Bulletin 73, 428–434.
Effects of elevated CO2 on the reproduction of two calanoid copepods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvVOit7k%3D&md5=f1fffc6178ead5fa322394b8008a5b62CAS | 23490345PubMed |

Mehrbach, C., Culberson, C. H., Hawley, J. E., and Pytkowicx, R. M. (1973). Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18, 897–907.
Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXhtFansLk%3D&md5=2ad6dd8f3ecd95e3af2a8fc66573547bCAS |

Melzner, F., Stange, P., Trübenbach, K., Thomsen, J., Casties, I., Panknin, U., Gorb, S. N., and Gutowska, M. A. (2011). Food supply and seawater CO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS One 6, e24223.
Food supply and seawater CO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yqsrjO&md5=761ee07ec5bb7ddc1a4b51a8ef9ec525CAS | 21949698PubMed |

Michaelidis, B., Ouzounis, C., Paleras, A., and Pörtner, H. O. (2005). Effects of long-term moderate hypercapnia on acid/base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 293, 109–118.
Effects of long-term moderate hypercapnia on acid/base balance and growth rate in marine mussels Mytilus galloprovincialis.Crossref | GoogleScholarGoogle Scholar |

Miles, H., Widdicombe, S., Spicer, J. I., and Hall-Spencer, J. (2007). Effects of anthropogenic seawater acidification on acid–base balance in the sea urchin Psammechinus miliaris. Marine Pollution Bulletin 54, 89–96.
Effects of anthropogenic seawater acidification on acid–base balance in the sea urchin Psammechinus miliaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntl2gsg%3D%3D&md5=628c3639d7e106407290f614bc0e1242CAS | 17083950PubMed |

Montagnes, D. J. S., Lowe, C. D., Roberts, E. C., Breckels, M. N., Boakes, D. E., Davidson, K., Keeling, P. J., Slamovits, C. H., Steinke, M., Yang, Z., and Watts, P. C. (2011). An introduction to the special issue: Oxyrrhis marina, a model organism? Journal of Plankton Research 33, 549–554.
An introduction to the special issue: Oxyrrhis marina, a model organism?Crossref | GoogleScholarGoogle Scholar |

Nielsen, L. T., Jakobsen, H. H., and Hansen, P. J. (2010). High resilience of two coastal plankton communities to twenty-first century seawater acidification: evidence from microcosm studies. Marine Biology Research 6, 542–555.
High resilience of two coastal plankton communities to twenty-first century seawater acidification: evidence from microcosm studies.Crossref | GoogleScholarGoogle Scholar |

Olson, M. B., and Kawaguchi, S. (2011). Workshop on ‘Impacts of Ocean Acidification on Zooplankton’. PICES Press 19, 28–29.

Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G.-K., Rodgers, K. B., Sabine, C. L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Totterdell, I. J., Weirig, M.-F., Yamanaka, Y., and Yool, A. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686.
Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCjsL%2FE&md5=ecb9c22a6dd796f57dab30648d0fe277CAS | 16193043PubMed |

Pagani, M., Huber, M., Liu, Z., Bohaty, S. M., Henderiks, J., Sijp, W., Krishnan, S., and DeConto, R. M. (2011). The role of carbon dioxide during the onset of antarctic glaciation. Science 334, 1261–1264.
The role of carbon dioxide during the onset of antarctic glaciation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFCms7vK&md5=ec0f9b82015fdffa88dce5fdb987dd96CAS | 22144622PubMed |

Pedersen, M. F., and Hansen, P. J. (2003). Effects of high pH on the growth and survival of six marine heterotrophic protists. Marine Ecology Progress Series 260, 33–41.
Effects of high pH on the growth and survival of six marine heterotrophic protists.Crossref | GoogleScholarGoogle Scholar |

Pörtner, H. (2008). Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecology Progress Series 373, 203–217.
Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view.Crossref | GoogleScholarGoogle Scholar |

Rose, J., Feng, Y., Gobler, C., Gutierrez, R., Hare, C., Leblanc, K., and Hutchins, D. (2009). Effects of increased pCO2 and temperature on the North Atlantic spring bloom. II. Microzooplankton abundance and grazing. Marine Ecology Progress Series 388, 27–40.
Effects of increased pCO2 and temperature on the North Atlantic spring bloom. II. Microzooplankton abundance and grazing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1SrtrjP&md5=0a125a3b7966973da880437c9ae4005fCAS |

Rossoll, D., Bermúdez, R., Hauss, H., Schulz, K. G., Riebesell, U., Sommer, U., and Winder, M. (2012). Ocean acidification-induced food quality deterioration constrains trophic transfer. PLOS One 7, e34737.
Ocean acidification-induced food quality deterioration constrains trophic transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtVOltrc%3D&md5=a01f34a1e76d358fb8d7968f26ca32e3CAS | 22509351PubMed |

Rossoll, D., Sommer, U., and Winder, M. (2013). Community interactions dampen acidification effects in a coastal plankton system. Marine Ecology Progress Series 486, 37–46.
Community interactions dampen acidification effects in a coastal plankton system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFSmtb3E&md5=9c86486d0417dc1a44f608fb88b43055CAS |

Royer, D. L. (2006). CO2-forced climate thresholds during the Phanerozoic. Geochimica et Cosmochimica Acta 70, 5665–5675.
CO2-forced climate thresholds during the Phanerozoic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1WmtbzM&md5=2555611fd44f0d1f7e8b6560c26e95b7CAS |

Schoo, K., Malzahn, A., Krause, E., and Boersma, M. (2013). Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore. Marine Biology 160, 2145–2155.
Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1GgtbbF&md5=d7a3ca31821e7af794482a859dfb7176CAS |

Sherr, E. B., and Sherr, B. F. (2002). Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81, 293–308.
Significance of predation by protists in aquatic microbial food webs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1Sgt7Y%3D&md5=ba96ab377847ecdcc10c2eddeb839728CAS | 12448728PubMed |

Sommer, U., Hansen, T., Blum, O., Holzner, N., Vadstein, O., and Stibor, H. (2005). Copepod and microzooplankton grazing in mesocosms fertilised with different Si : N ratios: no overlap between food spectra and Si : N influence on zooplankton trophic level. Oecologia 142, 274–283.
Copepod and microzooplankton grazing in mesocosms fertilised with different Si : N ratios: no overlap between food spectra and Si : N influence on zooplankton trophic level.Crossref | GoogleScholarGoogle Scholar | 15480805PubMed |

Sterner, R. W., and Elser, J. J. (2002). ‘Ecological Stoichiometry: the Biology of Elements from Molecules to the Biosphere.’ (Princeton University Press: Princeton)

Suffrian, K., Simonelli, P., Nejstgaard, J. C., Putzeys, S., Carotenuto, Y., and Antia, A. N. (2008). Microzooplankton grazing and phytoplankton growth in marine mesocosms with increased CO2 levels. Biogeosciences 5, 1145–1156.
Microzooplankton grazing and phytoplankton growth in marine mesocosms with increased CO2 levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlahu7jE&md5=49aa83640656dacd5fbfa2b2f98c976aCAS |

Tans, P., and Keeling, R. (2013). ‘Trends in Atmospheric Carbon Dioxide.’ (Global Greenhouse Gas Reference Network: Boulder.)

Thor, P., and Dupont, S. (2015). Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Global Change Biology 21, 2261–2271.
Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod.Crossref | GoogleScholarGoogle Scholar | 25430823PubMed |

Urabe, J., Togari, J. U. N., and Elser, J. J. (2003). Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore. Global Change Biology 9, 818–825.
Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore.Crossref | GoogleScholarGoogle Scholar |

van de Waal, D. B., Verschoor, A. M., Verspagen, J. M. H., van Donk, E., and Huisman, J. (2010). Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Frontiers in Ecology and the Environment 8, 145–152.
Climate-driven changes in the ecological stoichiometry of aquatic ecosystems.Crossref | GoogleScholarGoogle Scholar |

Yamada, Y., and Ikeda, T. (1999). Acute toxicity of lowered pH to some oceanic zooplankton. Plankton Biology and Ecology 46, 62–67.